This high council took on the role of chief judicial and legislative body of the local church and handled such things as excommunication trials and approval of all church spending. This high council became subordinate to the high council of Zion, which was organized in Jackson County, Missouri. Later, when other high councils were established in newly formed stakes of the church, the high council of Zion (first Kirtland, then Far West, Missouri and finally Nauvoo, Illinois) took on a role of "presiding" over the lesser high councils. (Cases tried in the high councils of outlying stakes were regularly appealed to the high council of Zion.) Most Latter Day Saint historians view the high council of Zion as distinct from a stake high council, as there is no "stake" at the "center place" of the tent of Zion. During Smith's lifetime, high council members were ordained high priests, but not given any priesthood keys.

In 1835, Smith created an additional "traveling high council" of twelve men to oversee the missionary work of the church. Like many early church leaders including the Three and Eight Witnesses of the Book of Mormon and, initially all church elders, the members of this traveling high council were known as "apostles." Later, as this council grew in importance, it became known as the Council or Quorum of the Twelve Apostles, and other church leaders ceased to be called apostles.

Thomas B. Marsh was the original president of the traveling high council which, in practice, was initially subordinate to the high council of Zion. For example, in 1838, when vacancies arose in the traveling high council, it was the presiding high council at Far West which voted on and filled the vacancies. Later, as the traveling high council evolved and began to be known as the Quorum of the Twelve Apostles, it acquired equal status with the presiding high council and both were subordinated to the First Presidency. When the high council of Zion was dissolved after the church members were expelled from Missouri, the high council organized at the new church headquarters in Nauvoo, Illinois, where it functioned as the presiding high council of the church, overseeing appeals from high councils in outlying stakes.